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Arthrospira Platensis As a Feasible Feedstock for Bioethanol Production

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Arthrospira Platensis As a Feasible Feedstock for Bioethanol Production applied sciences Review Arthrospira platensis as a Feasible Feedstock for Bioethanol Production Enrique Gonzalez Bautista and Céline Laroche * Institute Pascal, UMR CNRS 6602, University Clermont Auvergne, F-63000 Clermont-Ferrand, France; [email protected] * Correspondence: [email protected]; Tel.: +33-473-407-419 Abstract: In recent decades and to deal with the scarcity of fossil fuels, many studies have been developed in order to set up a sustainable biofuel production sector. This new sector must be efficient (high productivity), economically profitable (low production costs and therefore acceptable fuel prices), and ethical (low carbon balance, no competition with food resources). The production of bioethanol is based on the fermentation of reserve sugars, accumulated in the form of starch in microalgae and glycogen in cyanobacteria. The advantage of this bioenergy production route lies in the fact that the post-crop fermentation process is at the industrial stage since it has already been tested for many years for the production of bioethanol from agricultural resources. One of the most cultivated cyanobacteria is Arthrospira (“Spirulina”) and its production is also already at industrial scale. Depending on the cultivation conditions, this cyanobacteria is able to accumulate up to 65% DW (dry weight) of glycogen, making it a feasible feedstock for bioethanol production. The aim of this review is to provide a clear overview of these operating conditions for glycogen accumulation. Keywords: cyanobacteria; Arthrospira; glycogen Citation: Gonzalez Bautista, E.; Laroche, C. Arthrospira platensis as a 1. Introduction Feasible Feedstock for Bioethanol Faced with the decrease in available fossil fuel resources, their substitution with biofu- Production. Appl. Sci. 2021, 11, 6756. els like bioethanol or biodiesel could be a sustainable alternative [1]. Biofuel production https://doi.org/10.3390/app11156756 can be classified into different generations (from 1st, 2nd, 3rd, until the 4th G) based on the biomass feedstock and processing technology [2]. Each of them has different advan- Academic Editor: Francesca Scargiali tages and drawbacks. Meanwhile, 1st G biofuels use consolidated profitable processes, it competes for arable land with crop production [2]. In this context, 2nd G biofuels use Received: 30 June 2021 lignocellulosic by-products that do not compete for arable lands, nevertheless, most of Accepted: 22 July 2021 Published: 22 July 2021 the processes are not sustainable at an industrial scale [3]. On the other hand, 3rd and 4th G are based on low-input autotrophic microbial feedstock, especially microalgae and Chlorella Arthrospira Dunaliella, Botryococcus Haematococcus Publisher’s Note: MDPI stays neutral cyanobacteria (i.e., , , , or )[4,5]. with regard to jurisdictional claims in Innovative development of these processes can allow for the production of sustainable published maps and institutional affil- amounts of biofuel without competing for arable lands while fixing CO2 via photosynthe- iations. sis [6]. Indeed, the production of this type of biofuel is expected to be carbon negative both at the level of the raw material (fix atmospheric CO2) and process technology (low CO2 emission), helping reducing CO2 emissions and boost climate change mitigation [7]. Arthrospira platensis, also known as ‘spirulina’, is a filamentous photosynthetic cyanobac- terium composed of individual cells (about 8 µm in diameter), associated in trichomes Copyright: © 2021 by the authors. (about 500 µm length), which grows in subtropical alkaline lakes (pH 8.5 to 10) with an Licensee MDPI, Basel, Switzerland. ◦ This article is an open access article optimum temperature above 35 C[8–10]. This cyanobacterium has been studied world- distributed under the terms and wide for its application in pharmaceutical and health [11], cosmetics [12], nutrition [13], conditions of the Creative Commons bioremediation [14], and even in oxygen production for closed life support systems in Attribution (CC BY) license (https:// space [15]. Arthrospira platensis is commercialized in at least 22 countries and represents creativecommons.org/licenses/by/ about 60% of the global microalgal biomass production [5]. The main purpose of the indus- 4.0/). trial harvest of Arthrospira platensis is the extraction of proteins and bioactive molecules like Appl. Sci. 2021, 11, 6756. https://doi.org/10.3390/app11156756 https://www.mdpi.com/journal/applsci Appl. Sci. 2021, 11, 6756 2 of 15 phycocyanin among other compounds [16]. It is also consumed worldwide as a dietary supplement and considered as safe. However, attention has to be paid to the chelating properties of Spirulina species, which can lead to the fixation of heavy metals such as Al, Pb, Ba, Ni, Cd [17] or fluoride [18]. Nevertheless, this microorganism is also suitable for biofuel production (3rd generation) due to its fast growth, all year cultivation, and chemical composition (44.4% carbohydrates, 45% proteins, and 10% lipids and ashes) [19–21]. Its high carbon sequestration rate can reach 0.92 g/L/d, making it a feasible biofuel feed- stock [22,23]. In this context, the main biofuels produced by this cyanobacterium have been solid biofuel [24], bio-oil [25], and syngas [23]. Nevertheless, in recent years, a new ap- proach has been developed, which is the use of Arthrospira platensis storage polysaccharide (i.e., glycogen) for bioethanol production [26,27]. Glycogen (α-1,4 linked glucan) is a polymeric carbohydrate formed of glucose linked through α-1,4 and α-1,6 glycosidic bonds. This polysaccharide can be degraded via en- zymatic hydrolysis (saccharification) and fermented into bioethanol [28]. This energy- store polysaccharide is mainly formed in Arthrospira platensis as a response of nutrient- stressed conditions, and accumulated (up to 70% DW) in granules in the thylakoid mem- branes [29–31]. Once conditions are balanced, accumulated glycogen is hydrolyzed to produce energy for cell metabolism. This characteristic of Arthrospira platensis can be exploited to induce glycogen production for bioethanol production [32]. Different mod- ifications in culture medium and culture conditions of Arthrospira platensis can enhance glycogen production. This review aims to aggregate those operating conditions, allow- ing glycogen accumulation in order to have a better overview of the feasibility of using Arthrospira as a feedstock for bioethanol production. 2. Growth Requirements for Biomass Production The attempt in this first section is just to point out some key parameters influencing biomass production, while the objective of the review is to further highlight specific conditions promoting glycogen accumulation. Spirulina cultivation has been studied for a long time as it is probably the most cultivated photosynthetic microorganism worldwide. Under this generic name, several cyanobacteria may be encountered, especially species belonging to the genus Arthrospira. In a recent publication from Nowicka-Krawczyk et al. [33], phylogenetic analyses based on the 16S rRNA gene have allowed for a new classification of most of the commercially and bank deposited strains, including creation of a new genus under the name Limnospira to be established. However, this paper will not discriminate between these genus as it is not possible to clearly compare previous works with one or the other. Since the historical work of Zarrouk [34] on Spirulina maxima, numerous studies have been conducted focusing on abiotic factors such as light intensity, temperature, medium composition, pH, and salinity. Both indoor and outdoor conditions were studied in photobioreactors or open ponds. Subsequently, the individual or the combined effects of these environmental factors on biomass productivity are now well documented. It is well known that numerous parameters influence the growth or protein content of microalgae: light, temperature, salinity, CO2 addition, nutrient addition, inoculation size, stirring, pH, etc. [34–36] Most Arthrospira species currently grown in mass culture were isolated from alkaline and saline or brackish waters characterized by high levels of carbonate-bicarbonate and high pH levels. Zarrouk [34] determined the precise composition of the water in Lake Tchad Lake, a natural habitat for the Arthrospira maxima strain used in his study, allowing him to propose a synthetic medium that is still the basis of all cultivation media classically used for Arthrospira species. However, study of Cogne et al. [37] has shown that all compounds in Zarrouk medium were not necessary to support Arthrospira growth, thus proposing a simplification of the medium. The pH of these media varies between 8.3 and 10, as Zarrouk [34] showed that the growth rate was similar across this range. Belkin and Boussiba [38] confirmed that the maximal growth rate for Arthrospira was obtained in Appl. Sci. 2021, 11, 6756 3 of 15 the 9.5–9.8 range. When incubated at pH 7.0, the growth rate of Arthrospira was severely inhibited and was only 20% of that under the optimal conditions. Moreover, an external pH of 9.5 will lead to an internal pH of 7.5, which is the optimal pH for RuBisCo [39]. This high pH (>8) requirement clearly defines Arthrospira as an obligatory alkaliphile [40]. Generally, the waters populated by Arthrospira have a mean salinity of 37 g L−1. However, Arthrospira has been found at salinity levels ranging from 8.5 to 200 g L−1 and in at least one case, up to 270 g L−1 [41]. Salinity values used for laboratory or mass cultivations generally range from 22 to 60 g L−1. In nature, Arthrospira is found in permanent or temporary water bodies at relatively high temperatures. The optimal temperature for the cultivation of this organism is about 36 ◦C[34,42], but many studies at 30 ◦C can also be found. A detailed study on the response of a Spirulina strain marked M-2 was performed by Torzillo and Vonshak [43] and the optimal temperature for photosynthesis was 35 ◦C. However, many Arthrospira strains differ in their optimal growth temperature as well as in their sensitivity to extreme values. Vonshak [8] tested three different strains, one with a relatively low temperature optimum of 30–32 ◦C, while another grew well at a temperature of up to 40–42 ◦C.
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